How Mycorrhizal Associations Influence Orchid Distribution and Population Dynamics Taiqiang Li, Shimao Wu, Wenke Yang, Marc-André Selosse, Jiangyun Gao

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How Mycorrhizal Associations Influence Orchid Distribution and Population Dynamics Taiqiang Li, Shimao Wu, Wenke Yang, Marc-André Selosse, Jiangyun Gao How Mycorrhizal Associations Influence Orchid Distribution and Population Dynamics Taiqiang Li, Shimao Wu, Wenke Yang, Marc-André Selosse, Jiangyun Gao To cite this version: Taiqiang Li, Shimao Wu, Wenke Yang, Marc-André Selosse, Jiangyun Gao. How Mycorrhizal Associ- ations Influence Orchid Distribution and Population Dynamics. Frontiers in Plant Science, Frontiers, 2021, 12, pp.647114. 10.3389/fpls.2021.647114. hal-03235972 HAL Id: hal-03235972 https://hal.sorbonne-universite.fr/hal-03235972 Submitted on 26 May 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. REVIEW published: 07 May 2021 doi: 10.3389/fpls.2021.647114 How Mycorrhizal Associations Influence Orchid Distribution and Population Dynamics Taiqiang Li 1,2, Shimao Wu 1,2, Wenke Yang 1,2, Marc-André Selosse 1,2,3,4 and Jiangyun Gao 1,2* 1 Yunnan Key Laboratory of Plant Reproductive Adaptation and Evolutionary Ecology, Yunnan University, Kunming, China, 2 Laboratory of Ecology and Evolutionary Biology, Yunnan University, Kunming, China, 3 Institut de Systématique, Évolution, Biodiversité, UMR 7205, CNRS, MNHN, UPMC, EPHE, Muséum National d’Histoire Naturelle, Sorbonne Universités, Paris, France, 4 Department of Plant Taxonomy and Nature Conservation, Faculty of Biology, University of Gdańsk, Gdańsk, Poland Orchid distribution and population dynamics are influenced by a variety of ecological factors and the formation of holobionts, which play key roles in colonization and ecological community construction. Seed germination, seedling establishment, reproduction, and survival of orchid species are strongly dependent on orchid mycorrhizal fungi (OMF), with mycorrhizal cheating increasingly observed in photosynthetic orchids. Therefore, changes in the composition and abundance of OMF can have profound effects on orchid distribution and fitness. Network analysis is an important tool for the study of interactions between Edited by: Nadia Lombardi, plants, microbes, and the environment, because of the insights that it can provide into Università degli Studi di Napoli the interactions and coexistence patterns among species. Here, we provide a Federico II, Italy comprehensive overview, systematically describing the current research status of the Reviewed by: Lawrence W. Zettler, effects of OMF on orchid distribution and dynamics, phylogenetic signals in orchid–OMF Illinois College, United States interactions, and OMF networks. We argue that orchid–OMF associations exhibit Franck Richard, complementary and specific effects that are highly adapted to their environment. Such UMR5175 Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), specificity of associations may affect the niche breadth of orchid species and act as a France stabilizing force in plant–microbe coevolution. We postulate that network analysis is *Correspondence: required to elucidate the functions of fungal partners beyond their effects on germination Jiangyun Gao [email protected] and growth. Such studies may lend insight into the microbial ecology of orchids and provide a scientific basis for the protection of orchids under natural conditions in an efficient Specialty section: and cost-effective manner. This article was submitted to Plant Symbiotic Interactions, Keywords: orchid mycorrhizal fungi, orchid performance, complementary selection, environmental variables, a section of the journal evolutionary constraints, mycorrhizal networks, keystone taxa Frontiers in Plant Science Received: 29 December 2020 Accepted: 13 April 2021 Published: 07 May 2021 INTRODUCTION Citation: Mycorrhizal associations play a key role in generating and maintaining plant diversity. Such Li T, Wu S, Yang W, Selosse M-A and associations not only enhance the acquisition, transmission, and cycling of nutrients in Gao J (2021) How Mycorrhizal Associations Influence Orchid plants, but also mediate interactions among different plants and between plants and Distribution and Population Dynamics. non-mycorrhizal fungi (Tedersoo et al., 2020). A growing body of research suggests that Front. Plant Sci. 12:647114. mycorrhizal symbionts are important drivers of biogeographic patterns, distributions, community doi: 10.3389/fpls.2021.647114 dynamics, and the health of plants, mediated by their effects on dispersal and coexistence Frontiers in Plant Science | www.frontiersin.org 1 May 2021 | Volume 12 | Article 647114 Li et al. Roles of OMF in Orchid Distribution of species (Delavaux et al., 2019; Trivedi et al., 2020). For These clues strongly suggest that environmental factors may example, ectomycorrhizae (EcM) interact with pathogenic indirectly affect orchid distribution and population dynamics fungi to maintain community diversity (Chen et al., 2019a). by driving niche partitioning in OMF communities. Similarly, The family Orchidaceae is extremely diverse (with 28,000+ OMF can decompose carbon and nitrogen sources in soil species), widely distributed across highly heterogeneous organic matter and transfer them to the associated host orchids microenvironments, and exhibits large spatiotemporal variation (Rasmussen, 1995). In addition, orchids often share EcM with in population size (Givnish et al., 2016; Fay, 2018; Djordjević neighboring trees, hence orchid mycorrhiza may mediate the and Tsiftsis, 2020). A common feature of all orchids is their significant effect of vegetation types on orchid niche partitioning obligatory dependence on orchid mycorrhizal fungi (OMF), (Waterman and Bidartondo, 2008; Jacquemyn et al., 2016a). which makes the presence of suitable OMF or co-dispersal Orchid fungi are divided into OMF and orchid with partners a prerequisite for the establishment and non-mycorrhizal fungi (ONF) based on whether or not functional maintenance of orchid populations (Dearnaley et al., 2012; pelotons are present in cortical cells. OMF include at least 17 McCormick and Jacquemyn, 2014). Mycorrhizal symbiosis is families of basidiomycetes and five families or genera of especially important for plants associated with OMF and EcM, ascomycetes (Dearnaley, 2007; Dearnaley et al., 2012). as they often have high mycorrhizal specificityPõlme ( et al., Tulasnellaceae, Ceratobasidiaceae, and Serendipitaceae are most 2018). Most species of EcM fungi exhibit short-distance commonly known as rhizoctonia-type Basidiomycetes. dispersal and therefore, have limited ranges of distribution Basidiomycetes and Ascomycetes are relatively abundant in the (Sato et al., 2012; Tedersoo et al., 2020). Although the major tree roots of forest ecosystems and cultivated species worldwide mycorrhizal partners of terrestrial orchids appear to favor a (Cregger et al., 2018; Wang et al., 2019a; Trivedi et al., 2020), cross-scale distribution with specificity ranging from wide to and are commonly associated with orchids as well. Interestingly, very narrow (Jacquemyn et al., 2017; Swarts and Dixon, 2017), a large proportion of ascomycetes associated with orchids are comparatively little is known about the diversity and ONF. For example, Helotiales endophytes are the dominant biogeography of the associated mycorrhizae of epiphytic orchids. group of ONF associated with host orchids in different habitats Therefore, the interaction between OMF and orchids is a as well as major players in plant–fungus associations in a key factor determining orchid distribution and development, variety of forest ecotypes (Toju et al., 2013; Jacquemyn et al., and diversity of OMF has a strong impact on the niche and 2016a, 2017). Previous studies have identified more than 110 life cycle of host orchids. For instance, low OMF diversity genera of ONF, including 76 genera of ascomycetes and 32 and high heterogeneity in OMF community composition may genera of basidiomycetes (Ma et al., 2015). Although ONF lead to weak growth of orchid populations (Kaur et al., 2020). are often overlooked, recent studies have highlighted their Orchids exhibit astonishing morphological characteristics, importance in the promotion of orchid seed germination and such as labella and modified petals, that indicate their substantial performance as well as changes in the composition of key adaptability to the environment (Zhang et al., 2018). On one chemicals such as sugars. Moreover, they also play a role in hand, interactions with specific pollinators promote the mobilizing soil nutrients in the rhizosphere to improve orchid reproduction of orchids; on the other hand, symbiotic fungi viability and environmental adaptability, and serve as new are required for soil exploitation (Selosse, 2014). Greater sources of phytochemicals and bioactive substances to protect environmental heterogeneity and a wider range of resource the host from soil pathogens. Hence, these ONF provide the availability usually contribute to the increase of orchid species plants with promising medicinal and agricultural breeding diversity (Schödelbauerová et al., 2009; Traxmandlová et al., prospects (Chen et al., 2006; Yuan et al., 2009; Aly et al., 2018). Thus, untangling the role of environmental conditions 2010; Novotná et al., 2018; Sisti et al., 2019;
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